Phlebotomine sand flies employ an elaborate system of pheromone communication wherein males produce pheromones that attract other males to leks (thus acting as an aggregation pheromone) and females to the lekking males (sex pheromone). In addition, the type of pheromone produced varies among populations. Despite the numerous studies on sand fly chemical communication, little is known of their chemosensory genome. Chemoreceptors interact with chemicals in an organism’s environment to elicit essential behaviors such as the identification of suitable mates and food sources. Thus, they play important roles during adaptation and speciation. Major chemoreceptor gene families, odorant receptors (ORs), gustatory receptors (GRs) and ionotropic receptors (IRs) together detect and discriminate the chemical landscape. Here, we annotated the chemoreceptor repertoire in the genomes of Lutzomyia longipalpis and Phlebotomus papatasi, major phlebotomine vectors in the New World and Old World, respectively. Comparison with other sequenced Diptera revealed a large and unique expansion where over 80% of the ~140 ORs belong to a single, taxonomically restricted clade. We next conducted a comprehensive analysis of the chemoreceptors in 63 L. longipalpis individuals from four different locations in Brazil representing allopatric and sympatric populations and three sex-aggregation pheromone types (chemotypes). Population structure based on single nucleotide polymorphisms (SNPs) and gene copy number in the chemoreceptors corresponded with their putative chemotypes, and corroborate previous studies that identified multiple populations. Our work provides genomic insights into the underlying behavioral evolution of sexual communication in the L. longipalpis species complex in Brazil, and highlights the importance of accounting for the ongoing speciation in central and South American Lutzomyia that could have important implications for vectorial capacity.
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This research work was supported by funding from National Institute of Food and Agriculture, US Department of Agriculture (under HATCH Project 2353077000) to Z.S.
The data underlying the results presented in the study are all uploaded along with this m/s. and also available on https://doi.org/10.1101/2020.08.11.247155.
The preprint of this article is available from bioRxiv.
Hickner, Paul V.; Timoshevskaya, Nataliya; Nowling, Ronald J.; Labbé, Frédéric; Nguyen, Andrew D.; McDowell, Mary Ann; Spiegel, Carolina N.; and Syed, Zainulabeuddin, "Molecular Signatures of Sexual Communication in the Phlebotomine Sand Flies" (2020). Biology Faculty Publications. 204.
S1 Table. Accession numbers for SRAs and assigned chemotypes for the 63 L. longipalpis individual genome sequences used in the study. https://doi.org/10.1371/journal.pntd.0008967.s001
pntd.0008967.s002.xlsx (428 kB)
S2 Table. Chemoreceptor gene models for ORs, GRs and IRs for L. longipalpis and P. papatasi. https://doi.org/10.1371/journal.pntd.0008967.s002
pntd.0008967.s003.xlsx (349 kB)
S3 Table. SNPs in the 100 single-copy orthologs among the L. longipalpis field collections. https://doi.org/10.1371/journal.pntd.0008967.s003
pntd.0008967.s004.xlsx (56 kB)
S4 Table. Predicted gene copy number for 245 chemoreceptor genes in 63 L. longipalpis individuals. https://doi.org/10.1371/journal.pntd.0008967.s004
pntd.0008967.s005.xlsx (164 kB)
S5 Table. Gene models and confirmed absences for 522 genes based on manual annotations of the 63 de novo assemblies. https://doi.org/10.1371/journal.pntd.0008967.s005
pntd.0008967.s006.tif (2185 kB)
S1 Fig. Phylogenetic relationships among ORs in L. longipalpis, P. papatasi, A. gambiae, M. destructor and D. melanogaster. https://doi.org/10.1371/journal.pntd.0008967.s006
pntd.0008967.s007.tif (2660 kB)
S2 Fig. Phylogenetic relationships among GRs in L. longipalpis, P. papatasi, A. gambiae, M. destructor and D. melanogaster. https://doi.org/10.1371/journal.pntd.0008967.s007
pntd.0008967.s008.tif (1893 kB)
S3 Fig. Phylogenetic relationships among IRs in in L. longipalpis, P. papatasi, A. gambiae, M. destructor and D. melanogaster. https://doi.org/10.1371/journal.pntd.0008967.s008
pntd.0008967.s009.tif (3379 kB)
S4 Fig. pcadapt was used to identify loci associated with population structure based on SNPs in the exons of 245 chemoreceptor genes in 63 individuals. https://doi.org/10.1371/journal.pntd.0008967.s009
pntd.0008967.s010.tif (3884 kB)
S5 Fig. Two distinct conditions were identified producing a copy number of 1 (CN = 1), which is half the expected CN for a single-copy gene with two intact alleles. https://doi.org/10.1371/journal.pntd.0008967.s010